Retrograde regulation of synaptic vesicle endocytosis and recycling

Nature Neuroscience

Volumn 6, Issue 9, 2003, Pages 925-932

  Micheva, Kristina D ^a   Buchanan, JoAnn ^a   Holz, Ronald W ^b   Smith, Stephen J ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CYCLIC GMP; GREEN FLUORESCENT PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE;

ANIMAL CELL; ARTICLE; CELL ULTRASTRUCTURE; EMBRYO; ENDOCYTOSIS; EXOCYTOSIS; HIPPOCAMPUS; MEMBRANE VESICLE; NERVE CELL CULTURE; NERVE ENDING; NEUROTRANSMISSION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; SYNAPSE VESICLE;

ANIMALS; CELLS, CULTURED; CYCLIC GMP; ENDOCYTOSIS; HIPPOCAMPUS; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION; SYNAPTIC VESICLES;

EID: 0042861412     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1114     Document Type: Article

References (42)

1. Tao, H.W. & Poo, M. Retrograde signaling at central synapses. Proc. Natl. Acad. Sci. USA 98, 11009-11015 (2001).
2. Wilson, R.I. & Nicoll, R.A. Endocannabinoid signaling in the brain. Science 296, 678-682 (2002).
3. Prast, H. & Philippu, A. Nitric oxide as modulator of neuronal function. Prog. Neurobiol. 64, 51-68 (2001).
4. Arancio, O., Kandel, E.R. & Hawkins, R.D. Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′ -cGMP in cultured hippocampal neurons. Nature 376, 74-80 (1995).
5. Meffert, M.K., Calakos, N.C., Scheller, R.H. & Schulman, H. Nitric oxide modulates synaptic vesicle docking/fusion reactions. Neuron 16, 1229-1236 (1996).
6. Sporns, O. & Jenkinson, S. Potassium ion- and nitric oxide-induced exocytosis from populations of hippocampal synapses during synaptic maturation in vitro. Neuroscience 80, 1057-1073 (1997).
7. Klyachko, V.A., Ahern, G.P. & Jackson, M.B. cGMP-mediated facilitation in nerve terminals by enhancement of the spike after hyperpolarization. Neuron 31, 1015-1025 (2001).
8. Micheva, K.D., Holz, R.W. & Smith, S.J. Regulation of presynaptic phosphatidylinositol 4,5-biphosphate by neuronal activity. J. Cell Biol. 154, 355-368 (2001).
9. Cremona, O. & De Camilli, P. Phosphoinositides in membrane traffic at the synapse. J. Cell Sci. 114, 1041-1052 (2001).
10. Martin, T.F.J. PI(4,5)P(2) regulation of surface membrane traffic. Curr. Opin. Cell Biol. 13, 493-499 (2001).
11. Osborne, S.L., Meunier, F.A. & Schiavo, G. Phosphoinositides as key regulators of synaptic function. Neuron 32, 9-12 (2001).
12. Rao, A., Kim, E., Sheng, M. & Craig, A.-M. Heterogeneity in the molecular composition of excitatory postsynaptic sites during development of hippocampal neurons in culture. J. Neurosci. 18, 1217-1229 (1998).
13. Wendland, B. et al. Existence of nitric oxide synthase in rat hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA 91, 2151-2155 (1994).
14. Burette, A., Zabel, U., Weinberg, R. J., Schmidt, H.H.H.W. & Valtschanoff, J.G. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J. Neurosci. 22, 8961-8970 (2002).
15. Son, H. et al. Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87, 1015-1023 (1996).
16. De Camilli, P., Slepnev, V.I., Shupliakov, O. & Brodin, L. Synaptic vesicle endocytosis. in Synapses (eds. Cowan, M.W., Sudhof, T.C. & Stevens, C.F.) 217-274 (The Johns Hopkins Univ. Press, Baltimore, MD, 2001).
17. Li, Z. & Murthy, V.N. Visualizing postendocytic traffic of synaptic vesicles at hippocampal synapses. Neuron 31, 593-605 (2001).
18. Betz, W.J., Mao, F. & Bewick, G.S. Activity-dependent fluorescent staining and destaining of living motor nerve terminals. J. Neurosci. 12, 363-375 (1992).
19. Ryan, T.A. Presynaptic imaging techniques. Curr. Opin. Neurobiol. 11, 544-549 (2001).
20. Khvotchev, M. & Südhof, T. Newly synthesized phosphatidylinositol phosphates are required for synaptic norepinephrine but not glutamate or 7-aminobutyric acid (GABA) release. J. Biol. Chem. 273, 21451-21454 (1998).
21. 3H]inositol-labeled phosphoinositide pools. J. Cell Biol. 143, 501-510 (1998).
22. Paterson, H.F. et al. Phospholipase C delta 1 requires a pleckstrin homology domain for interaction with the plasma membrane. Biochem. J. 312, 661-666 (1995).
23. Ryan, T.A. & Smith, S.J. Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983-989 (1995).
24. Hokin, L. & Hokin, M.R. Biochim. Biophys. Acta 84, 563-575 (1964).
25. Eichberg, J. & Dawson, R.M. Polyphosphoinositides in myelin. Biochem. J. 96, 644-650 (1965).
26. Klingauf, J., Kavalali, E.T. & Tsien, R.W. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394, 581-585 (1998).
27. Sankaranarayanan, S. & Ryan, T.A. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci. 4, 129-136 (2001).
28. Berridge, M.J., Lipp, P. & Bootman, M.D. The versatility and universatility of calcium signalling. Nat. Rev. Mol. Cell Biol. 1, 11-21 (2000).
29. Wu, L., Bauer, C.S., Zhen, X., Xie, C. & Yang, J. Dual regulation of voltage-gated calcium channels by Ptdlns(4,5)P2. Nature 419, 947-952 (2002).
30. Gaidarov, I. & Keen, J.H. Phosphoinositide-AP-2 interactions required for targeting to plasma membrane clathrin-coated pits. J. Cell Biol. 146, 755-764 (1999).
31. Ford, M.G.J. et al. Simultaneous binding of Ptdlns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291, 1051-1055 (2001).
32. Itoh, T. et al. Role of the ENTH domain in phosphatidylinositol-4,5,-biphosphate binding and endocytosis. Science 291, 1047-1051 (2001).
33. Lin, H.C. & Gilman, A.G. Regulation of dynamin I GTPase activity by G protein beta gamma subunits and phosphatidylinositol 4,5-biphosphate. J. Biol. Chem. 271, 27979-27982 (1996).
34. Zheng, J. et al. Identification of the binding site for acidic phospholipids on the PH domain of dynamin: Implications for stimulation of GTPase activity. J. Mol. Biol. 255, 14-21 (1996).
35. Cremona, O. et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188 (1999).
36. Rozelle, A.L. et al. Phosphatidylinositol 4,5-biphosphate induces actin-based movement of raft-enriched vesicles through WASP-Arp2/3. Curr. Biol. 10, 311-320 (2000).
37. Wenk, M.R. et al. PIP kinase Iγ is the major PI(4,5)P2 synthesizing enzyme at the synapse. Neuron 32, 79-88 (2001).
38. Guo, J. et al. Phosphatidylinositol 4-kinase type IIα is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl. Acad. Sci. USA 100, 3995-4000 (2003).
39. McPherson, P.S. et al. A presynaptic inositol-5-phosphatase. Nature 379, 353-357 (1996).
40. 2+]i responses are negatively modulated via a cGMP-dependent protein kinase I pathway. J. Biol. Chem. 270, 22277-22282 (1995).
41. Goslin, K., Asmussen, H. & Banker, G. Rat hippocampal neurons in low-density culture. in Culturing Nerve Cells (eds. Banker, G. & Goslin, K.) 339-370 (MIT Press, Cambridge, Massachusetts, 1998).
42. Xia, Z., Dudek, H., Miranti, C.K. & Greenberg, M.E. Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism. J. Neurosci. 16, 5425-5436 (1996).